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The defeat means that Mr Cameron’s attempts to weaken rules forcing ministers and officials to be neutral in the purdah period in the weeks before the historic vote have failed.
David Cameron has suffered the first House of Commons defeat of his new Government at the hands of his own MPs on Europe.
The Prime Minister was defeated for the first time as a majority Tory Prime Minister, losing a vote on the purdah rules for the European Union referendum 312 to 285, majority 27.
In all 37 Conservative MPs – including Graham Brady, the chairman of the 1922 committee of Tory backbenchers and former ministers Sir Gerald Howarth, Tim Loughton and David Jones – rebelled.
The rebellion was a bigger number than in June when 27 Conservative MPs voted against the Government on a similar amendment – although on that occasion ministers avoided defeat as Labour abstained.
The defeat capped a difficult evening as his ministers also conceded new restrictions which will stop him ordering a snap referendum.
Labour said Mr Cameron had been “humiliated” by own Eurosceptic MPs, who had joined forces with the SNP and Labour.
The defeat means that the Governments attempts over the past few months to weaken rules forcing ministers and officials to be neutral in the weeks before the historic vote have failed.
Instead ministers will have to submit a list of subject areas that they hope to raise during the official campaign to Parliament, where MPs now have a veto.
In the face of another rebellion the Government also agreed to an amendment proposed by Tory MP Bernard Jenkin to give four months’ notice before holding the referendum.
Steve Baker MP, the leader of the rebels, said: “I regret it was necessary to force a division but I believe that we now have the right outcome. The Government has the framework within which to bring forward any necessary narrow exemptions to the purdah regime.
“This is far better than the proposed watering down of the scope of purdah. tThis was a limited disagreement and we are now looking forward to moving on.”
Mr Jenkin added: “We won the argument for a fairer referendum and i hope that the Government wil now accept that this is what Parliament wants.”
Owen Paterson, a former Tory Cabinet minister in Mr Cameron’s last Government, added: “The referendum is about the future of who runs our country. I am delighted that Parliament has voted to reinstate purdah so we can have a transparent national debate.”
Hilary Benn MP, the Shadow Foreign Secretary, said Mr Cameron had been “humiliated”. He said: “This is a humiliating defeat for David Cameron, with members from all sides of the House supporting Labour’s approach to purdah, which ensures fairness in the conduct of the referendum campaign while permitting normal government business to take place.
“The Government should never have rushed through its flawed plans to play fast and loose with the rules on the referendum.”
Earlier there were bitter clashes about the Whitehall “purdah” rules banning the use of public money to promote the Government’s view on Europe in the final 28 days of a referendum campaign.
Sir Edward Leigh said ministers were offering “legalistic claptrap” in a bid to avoid Commons defeat over rules for the EU referendum.
He said: “What the Government is seeking to do through these amendments is to manage that legal risk.”
Others mocked a claim from Mr Lidington that individual MPs might be gagged during the referendum campaign under exiting purdah rules.
John Redwood, a former Tory Cabinet minister, said it was well known that MPs “join in referendum campaigns, by elections and local elections, and they do so as politicians”.
Earlier the Electoral Commission, which will oversee the referendum, had boosted the rebels by ruling that it supported the reinstatement of the rules on Whitehall purdah ahead of the referendum.
A Labour party spokesman said ministers were trying to “pull a fast one” by adopting “skimmed milk” purdah restrictions, rather than the “full fat” version preferred by Labour which existed before last year’s Scottish referendum.